Morphological Correlations of Human and Monkey Frontal Lobe

Abstract

The prefrontal cortex has long been regarded as a major integrative subdivision of the forebrain. In particular, the results of clinical, experimental, and neuroimaging studies have established a role for this region in a variety of functions, such as planning and sequencing, emotional significance, attention, and representational memory. One question that arises is whether the discrete functions ascribed to the prefrontal cortex represent circumscribed processes at the neural level — that is, are subserved by a specific cortical subsector — or are dependent on the interactions of different prefrontal regions. A broader issue is the degree to which functions that appear to have the prefrontal cortex as a critical focus depend upon interactions with post-Rolandic cortices. Knowledge of the morphological characteristics of the prefrontal cortex may provide further insight into the underlying nature of these cognitive-behavioral functions. Therefore, in examining a complex process such as decision-making from a neural perspective, it may be beneficial to consider functional components in the context of cellular as well as connectional features of prefrontal areas.

A large amount of comparative research in monkeys on both structural and functional aspects of the prefrontal cortex has been carried out in recent years. Although the prefrontal cortex in humans has been shown to have a role in higher cognitive functions on the basis of clinical and neuroimaging techniques, such studies do not permit a detailed analysis of morphological underpinnings. There is a need to correlate data from human and monkey studies to gain a better understanding of cortical function. Several investigators have parcellated the human frontal cortex on the basis of architectonic features (e.g., Brodmann 1909; von Economo and Koskinas 1925; Sarkissov et al. 1955), and similar studies have been carried out in monkeys (e.g., Brodmann 1905; Vogt and Vogt 1919; Walker 1940). The cortical maps in humans and monkeys share basic similarities; however, they differ in regard to boundaries of specific areas and the numbers of areas identified. In an attempt to reconcile these differences, prefrontal areas have been examined from the perspective of progressive architectonic differentiation. Accordingly, the prefrontal cortex in both humans and monkeys can be organized in terms of two parallel trends. Thus, in both species a mediodorsal trend can be traced from the archicortex (hippocampal rudiment) on the medial surface around the corpus callosum. This trend proceeds through prosiocortical areas 24, 32, and 25, extends into medial areas 8B, 9B, and mediodorsal area 10, passes to dorsal areas 10 and 46, and ends in dorsal areas 9A/46 and 8A. A basoventral trend originates in the paleocortex (olfactory tubercle) on the orbital surface. This trend extends from orbital proisocortex to areas 13, 14, and 11, progresses through area 47/12 and ventral areas 10 and 46, and finally reaches areas 9/46, 8A, as well as areas 45 and 44 (Petrides and Pandya 1995).

Progressive architectonic differentiation has been correlated with cortical connections in monkeys (Pandya and Yeterian 1985; Barbas and Pandya 1989). The intrinsic connections of the prefrontal cortex are organized in a specific manner. Within each trend a given area projects in two directions, to a more differentiated region on the one hand and to a less differentiated region on the other. Likewise, long connections between prefrontal cortices and post-Rolandic sensory association regions — somatosensory, visual, and auditory — reflect progressive architectonic organization. Within each trend, frontal areas are related most strongly to post-Rolandic areas that appear to have a similar level of architectonic differentiation.

The data on the progressive architecture and intrinsic connectivity of the prefrontal cortex suggest a neural substrate for the continual interchange of information between proisocortices on the one hand and highly differentiated isocortices on the other. Conceptually with regard to decision-making, this intrinsic prefrontal circuitry may be thought of as providing systematic linkages between regions engaged in emotion (e.g., areas 13, 14, and 11) and motivation (e.g., areas 25 and 32); planning, sequencing and working memory (e.g., areas 9, 10 and 46); and attention (e.g., area 8). At the same time, the long association connections between the prefrontal cortex and post-Rolandic regions are integrated with the intrinsic prefrontal circuitry in a systematic manner, thereby allowing post-Rolandic influences such as complex long-term memories and immediate perceptions to play a role in ongoing decisional processes.